Please wait a minute...
Journal of Integrative Agriculture  2021, Vol. 20 Issue (7): 1849-1857    DOI: 10.1016/S2095-3119(20)63276-2
Special Issue: 植物抗病遗传合辑Plant Disease-resistance Genetics
Plant Protection Advanced Online Publication | Current Issue | Archive | Adv Search |
The TaFIM1 gene mediates wheat resistance against Puccinia striiformis f. sp. tritici and responds to abiotic stress
SHI Bei-bei1, WANG Juan1, 2, GAO Hai-feng3, ZHANG Xiao-juan1, WANG Yang1, MA Qing1 
1 State Key Laboratory of Crop Stress Biology for Arid Areas, Northwest A&F University, Yangling 712100, P.R.China
2 School of Life Science, Shanxi Datong University, Datong 037009, P.R.China
3 Institute of Plant Protection, Xinjiang Academy of Agricultural Sciences/Key Laboratory of Integrated Pest Management on Crop in Northwestern Oasis, Ministry of Agriculture and Rural Affairs, Urumqi 830091, P.R.China
Download:  PDF in ScienceDirect  
Export:  BibTeX | EndNote (RIS)      
摘要  

丝束蛋白(fimbrin)是肌动蛋白细胞骨架的调节因子,参与并控制多种组织和细胞的生理生化和发育过程。然而,fimbrin在对病原菌防御中,特别是在小麦抗条锈病中的作用研究匮乏,其机制尚待阐明。本研究以小麦品种水源11(Suwon 11)与条锈菌(Puccinia striiformis f. sp. triticiPst)生理小种CYR23组成非亲和互作,与生理小种CYR31组成成亲和互作,利用实时荧光定量 PCR 技术(qRT-PCR)对TaFIM1基因参与小麦抗条锈病的功能进行初步分析;对在非生物胁迫和施用外源激素处理TaFIM1基因的表达特征进行分析;通过病毒诱导的基因沉默(BSMV-VIGS)技术,验证TaFIM1在小麦抗条锈病中的功能。获得以下研究结果:TaFIM1在非亲和互作中的表达量显著上调,且在48 h表达量达到峰值,是对照0 h的6.0倍;在亲和互作中,TaFIM1的表达量无明显变化。TaFIM1能够响应不同非生物胁迫,在高温(Hot)、低温(Cool)、盐(NaCl)和干旱(PEG6000)胁迫下诱导TaFIM1基因表达量上调。BSMV-VIGS试验结果显示,借助大麦条纹花叶病毒对TaFIM1基因进行诱导沉默。对沉默成功的小麦植株分别接种条锈菌CYR23和CYR31。在非亲和互作中,沉默植株的抗病性降低,叶片上出现少量的夏孢子堆;在亲和互作中,与对照相比,叶片上的夏孢子堆数量增加,沉默植株的感病性增强。组织学观察发现,在48 h和120 h,TaFIM1沉默植株叶片中菌丝分支数和菌丝长度高于对照,在120 h基因沉默植株叶片中菌落面积显著高于对照组,表明TaFIM1沉默后小麦植株与对照相比感病性增强,进一步说明TaFIM1参与植物的抗病性。因此,TaFIM1与植物抗病性相关,在小麦抵抗条锈病的侵染过程中响应正调控作用。本研究为理解fimbrin在小麦中的作用提供了新的见解。




Abstract  
Fimbrin, a regulator of actin cytoskeletal dynamics that participates in numerous physiological and biochemical processes, controls multiple developmental processes in a variety of tissues and cell types.  However, the role of fimbrin in pathogen defense of wheat and the mechanisms have not been well studied.  Here, we investigated that the expression of TaFIM1 gene of wheat was significantly induced in response to avirulent race of Puccinia striiformis f. sp. tritici (Pst) and silencing of TaFIM1 by virus-induced gene silencing method.  The results show that silencing of TaFIM1 resulted in a reduction of resistance against the stripe rust indicated by both phenotypes and a histological examination of Pst growth.  Additionally, the expression level of TaFIM1 gene was up-regulated under abiotic stresses.  These findings suggest that TaFIM1 functions as a positive regulator of pathogen resistance of wheat plants and response to abiotic stress.  Our work may show new light on understanding the roles of fimbrin in wheat. 
Keywords:  wheat        Puccinia striiformis f. sp. tritici        fimbrin        disease resistance        abiotic stress  
Received: 03 March 2020   Accepted:
Fund: The research was supported by the National Natural Science Foundation of China (31571960), the NSFC-Xinjiang Joint Fund, China (U1903110) and the 111 Project from the Ministry of Education of China (B07049).
Corresponding Authors:  Correspondence WANG Yang, E-mail: wangyang2006@nwsuaf.edu.cn; MA Qing, E-mail: maqing@nwsuaf.edu.cn   
About author:  SHI Bei-bei, E-mail: shibeibei@nwafu.edu.cn

Cite this article: 

SHI Bei-bei, WANG Juan, GAO Hai-feng, ZHANG Xiao-juan, WANG Yang, MA Qing. 2021. The TaFIM1 gene mediates wheat resistance against Puccinia striiformis f. sp. tritici and responds to abiotic stress. Journal of Integrative Agriculture, 20(7): 1849-1857.

Adams A E M, Botstein D, Drubin D G. 1991. Requirement of yeast fimbrin for actin organization and morphogenesis in vivo. Nature, 354, 404–408.
Adams A E M, Shen W Y, Lin C S, Leavitt J, Matsudaira P. 1995. Isoformspecific complementation of the yeast sac6 null mutation by human fimbrin. Molecular and Cellular Biology, 15, 69–75.
Alazem M, Lin N S. 2015. Roles of plant hormones in the regulation of host-virus interactions. Molecular Plant Pathology, 16, 529–540.
Beddow J M, Pardey P G, Chai Y, Hurley T M, Kriticos D J, Braun H J, Park R F, Cuddy W S, Yonow T. 2015. Research investment implications of shifts in the global geography of wheat stripe rust. Nature Plants, 1, 1–32.
Chen P D, Qi L L, Zhou B, Zhang S Z, Liu D J. 1995. Development and molecular cytogenetic analysis of wheat-Haynaldia villosa 6VS/6AL translocation lines specifying resistance to powdery mildew. Theoretical and Applied Genetics, 91, 1125–1128.
Cruz-Ortega R. 1997. cDNA clones encoding 1,3-beta-glucanase and a fimbrin-like cytoskeletal protein are induced by AI toxicity in wheat roots. Plant Physiology, 114, 1453–1460.
Dangl J L, Horvath D M, Staskawicz B J. 2013. Pivoting the plant immune system from dissection to deployment. Science, 341, 746–751.
Day B, Henty J L, Porter K J, Staiger C J. 2011. The pathogen-actin connection: A platform for defense signaling in plants. Annual Review of Phytopathology, 49, 483–506.
Dodds P N, Rathjen J P. 2010. Plant immunity: Towards an integrated view of plant-pathogen interactions. Nature Reviews Genetics, 11, 539–548.
Dong Z, Hegarty J M, Zhang J, Zhang W, Dubcovsky J. 2017. Validation and characterization of a QTL for adult plant resistance to stripe rust on wheat chromosome arm 6BS (Yr78). Theoretical and Applied Genetics, 130, 2127–2137.
Fujiwara I, Takahashi S, Tadakuma H, Funatsu T, Ishiwata S I. 2002. Microscopic analysis of polymerization dynamics with individual actin filaments. Nature Cell Biology, 4, 666–673.
Galá J E, Collmer A. 1999. Type III secretion machines: Bacterial devices for protein delivery into host cells. Science, 284, 1322–1328.
Gessese M, Bariana H, Wong D, Hayden M, Bansal U. 2019. Molecular mapping of stripe rust resistance gene Yr81 in a common wheat landrace Aus27430. Plant Disease, 103, 1166–1171.
Hein I, Barciszewska-Pacak M, Hrubikova K, Williamson S, Dinesen M, Soenderby I E, Sundar S, Jarmolowski A, Shirasu K, Lacomme C. 2005. Virus-induced gene silencing-based functional characterization of genes associated with powdery mildew resistance in barley. Plant Physiology, 138, 2155–2164.
Henty-Ridilla J L, Shimono M, Li J, Chang J H, Day B, Staiger C J. 2013. The plant actin cytoskeleton responds to signals from microbe-associated molecular patterns. PLoS Pathogens, 9, 32–45.
Huang G T, Ma S L, Bai L P, Zhang L, Ma H, Jia P, Liu J, Zhong M, Guo Z F. 2012. Signal transduction during cold, salt, and drought stresses in plants. Molecular Biology Reports, 39, 969–987.
Jones J D G, Dangl J L. 2006. The plant immune system. Nature, 444, 323–329.
Kang Z S, Li Z Q. 1984. Discovery of a normal T. type new pathogenic strain to Lovrin 10. Journal of Northwest Sci-tech University of Agriculture and Forestry (Natural Science Edition, 4, 18–28. (in Chiense)
Klein M G, Shi W, Ramagopal U, Tseng Y, Wirtz D, Kovar D R, Staiger C J, Almo S C. 2004. Structure of the actin crosslinking core of fimbrin. Structure, 12, 999–1013.
Kovar D R, Gibbon B C, Staiger M C J. 2001. Fluorescently-labeled fimbrin decorates a dynamic actin filament network in live plant cells. Planta, 213, 390–395.
Lazniewska J, Macioszek V K, Kononowicz A K. 2012. Plant-fungus interface: The role of surface structures in plant resistance and susceptibility to pathogenic fungi. Physiological & Molecular Plant Pathology, 78, 24–30.
Li J, Henty-Ridilla J L, Staiger B H, Day B, Staiger C J. 2015. Capping protein integrates multiple MAMP signaling pathways to modulate actin dynamics during plant innate immunity. Nature Communications, 6, 7206–7215.
Liu B. 2011. The Plant Cytoskeleton. Springer, New York.
Macho A P, Zipfel C. 2015. Targeting of plant pattern recognition receptor-triggered immunity by bacterial type-III secretion system effectors. Current Opinion in Microbiology, 23, 14–22.
Marais F, Marais A, McCallum B, Pretorius Z. 2009. Transfer of leaf rust and stripe rust resistance genes Lr62 and Yr42 from Aegilops neglecta Req. ex Bertol. to common wheat. Crop Science, 49, 871–879.
Marais G F, McCallum B, Marais A S. 2006. Leaf rust and stripe rust resistance genes derived from Aegilops sharonensis. Euphytica, 149, 373–380.
Marais G F, Pretorius Z A, Marais A S, Wellings C R. 2003. Transfer of rust resistance genes from Triticum species to common wheat. South African Journal of Plant and Soil, 20, 193–198.
Minsavage G V, Dahlbeck D, Whalen M C, Kearney B, Bonas U, Staskawicz B J. 1990. Gene-for-gene relationships specifying disease resistance in Xanthomonas campestris pv vesicatoria-pepper interactions. Molecular Plant Microbe Interactions, 3, 41–48.
Miyakawa T, Shinomiya H, Yumoto F. 2012. Different Ca2+-sensitivities between the EF-hands of T- and L-plastins. Biochemical & Biophysical Research Communications, 429, 137–141.
Niirnberger T, Nennstiel D, Jabs T, Sacks W R, Hahlbrock K, Scheel D. 1994. Highaffinity binding of a fungal oligopeptide elicitor to parsley plasma membranes triggers multiple defense responses. Cell, 78, 60–72.
Ouellet F, Carpentier E, Cope M J T, Monroy A F, Sarhan F. 2001. Regulation of a wheat actin-depolymerizing factor during cold acclimation. Plant Physiology, 125, 360–368.
Petty I T, French R, Jones R W, Jackson A O. 1990. Identification of barley stripe mosaic virus genes involved in viral RNA replication and systemic movement. The EMBO Journal, 9, 3453–3457.
Qi T, Wang J, Sun Q X, Day B, Guo J, Ma Q. 2017. TaARPC3, contributes to wheat resistance against the stripe rust fungus. Frontiers in Plant Science, 8, 1–13.
Shinomiya H. 2012. Plastin family of actin-bundling proteins: its functions in leukocytes, neurons, intestines, and cancer. International Journal of Cell Biology, 2012, 213–235.
Singh R P, Singh P K, Rutkoski J, Hodson D P, He X, JøRgenssen L N, Hovmøller M S, Espino J H. 2016. Disease impact on wheat yield potential and prospects of genetic control. Annual Review of Phytopathology, 54, 615–635.
Su H, Zhu J S, Cai C, Pei W K, Wang J J, Dong H J, Ren H Y.  2012. Fimbrin1 is involved in lily pollen tube growth by stabilizing the actin fringe. The Plant Cell, 24, 4539–4554.
Sugiyama Y, Nagashima Y, Wakazaki M, Sato M, Toyooka K, Fukuda H, Oda Y. 2019. A Rho-actin signaling pathway shapes cell wall boundaries in Arabidopsis xylem vessels. Nature Communications, 10, 468–480.
Sun G Z, Feng C J, Guo J, Zhang A C, Xu Y L, Wang Y, Day B, Ma Q. 2019. The tomato Arp2/3 complex is required for resistance to the powdery mildew fungus Oidium neolycopersici. Plant, Cell & Environment, 10, 135–149.
Sun H, Qiao Z, Chua K P, Tursic A, Liu X, Gao Y G. 2018. Profilin negatively regulates formin-mediated actin assembly to modulate PAMP-triggered plant immunity. Current Biology, 26, 177–195.
Uauy C, Brevis J C, Chen X, Khan I, Jackson L, Chicaiza O, Distelfeld A, Fahima T, Dubcovsky J. 2005. High-temperature adult-plant (HTAP) stripe rust resistance gene Yr36 from Triticum turgidum ssp. dicoccoides is closely linked to the grain protein content locus Gpc-B1. Theoretical and Applied Genetics, 112, 97–105.
Vidali L, Mckenna S T, Hepler P K. 2001. Actin polymerization is essential for pollen tube growth. Molecular Biology of the Cell, 12, 2534–2545.
Wang J, Wang Y, Liu X J, Xu Y L, Ma Q. 2016. Microtubule polymerization functions in hypersensitive response and accumulation of H2O2 in wheat induced by the stripe rust. Biomed Research International, 3, 1–7.
Wang W, Wen Y, Berkey R, Xiao S. 2009. Specific targeting of the Arabidopsis resistance protein RPW8.2 to the interfacial membrane encasing the fungal haustorium renders broad-spectrum resistance to powdery mildew. The Plant Cell, 21, 2898–2913.
Wang X, Tang C, Zhang H, Xu J R, Liu B, Lv J, Han D, Huang L, Kang Z S. 2011. TaDAD2, a negative regulator of programmed cell death, is important for the interaction between wheat and the stripe rust fungus. Molecular Plant Microbe Interactions, 24, 79–90.
Wang X, Wang X, Feng H, Tang C, Bai P, Wei G, Huang L L, Kang Z S. 2012. TaMCA4, a novel wheat metacaspase gene functions in programmed cell death induced by the fungal pathogen Puccinia striiformis f. sp. tritici. Molecular Plant Microbe Interactions, 25, 755–764.
Wellings C R. 2011. Global status of stripe rust: A review of historical and current threats. Euphytica, 179, 129–141.
Yiping Q I, Tsuda K, Glazebrook J, Katagiri F. 2011. Physical association of pattern-triggered immunity (PTI) and effector-triggered immunity (ETI) immune receptors in Arabidopsis. Molecular Plant Pathology, 12, 702–708.
Zhang B, Hua Y, Wang J, Huo Y, Shimono M, Day B, Ma Q. 2017. TaADF4, an actin-depolymerizing factor from wheat, is required for resistance to the stripe rust pathogen Puccinia striiformis f. sp. tritici. Plant Journal, 89, 121–130.
Zhang M, Zhang R, Qu X, Huang S. 2016. Arabidopsis FIM5 decorates apical actin filaments and regulates their organization in the pollen tube. Journal of Experimental Botany, 67, 3407–3417.
Zheng Z, Gao T, Zhang Y, Hou Y, And J W, Zhou M. 2014. FgFim, a key protein regulating resistance to the fungicide js399-19, asexual and sexual development, stress responses and virulence in Fusarium graminearum. Molecular Plant Pathology, 15, 488–499.
[1] Zihui Liu, Xiangjun Lai, Yijin Chen, Peng Zhao, Xiaoming Wang, Wanquan Ji, Shengbao Xu. Selection and application of four QTLs for grain protein content in modern wheat cultivars[J]. >Journal of Integrative Agriculture, 2024, 23(8): 2557-2570.
[2] Gensheng Zhang, Mudi Sun, Xinyao Ma, Wei Liu, Zhimin Du, Zhensheng Kang, Jie Zhao. Yr5-virulent races of Puccinia striiformis f. sp. tritici possess relative parasitic fitness higher than current main predominant races and potential risk[J]. >Journal of Integrative Agriculture, 2024, 23(8): 2674-2685.
[3] Wenjie Yang, Jie Yu, Yanhang Li, Bingli Jia, Longgang Jiang, Aijing Yuan, Yue Ma, Ming Huang, Hanbing Cao, Jinshan Liu, Weihong Qiu, Zhaohui Wang. Optimized NPK fertilizer recommendations based on topsoil available nutrient criteria for wheat in drylands of China[J]. >Journal of Integrative Agriculture, 2024, 23(7): 2421-2433.
[4] Yibo Hu, Feng Qin, Zhen Wu, Xiaoqin Wang, Xiaolong Ren, Zhikuan Jia, Zhenlin Wang, Xiaoguang Chen, Tie Cai. Heterogeneous population distribution enhances resistance to wheat lodging by optimizing the light environment[J]. >Journal of Integrative Agriculture, 2024, 23(7): 2211-2226.
[5] Bingli Jiang, Wei Gao, Yating Jiang, Shengnan Yan, Jiajia Cao, Litian Zhang, Yue Zhang, Jie Lu, Chuanxi Ma, Cheng Chang, Haiping Zhang. Identification of P-type plasma membrane H+-ATPases in common wheat and characterization of TaHA7 associated with seed dormancy and germination[J]. >Journal of Integrative Agriculture, 2024, 23(7): 2164-2177.
[6] Yongchao Hao, Fanmei Kong, Lili Wang, Yu Zhao, Mengyao Li, Naixiu Che, Shuang Li, Min Wang, Ming Hao, Xiaocun Zhang, Yan Zhao.

Genome-wide association study of grain micronutrient concentrations in bread wheat [J]. >Journal of Integrative Agriculture, 2024, 23(5): 1468-1480.

[7] Zhikai Cheng, Xiaobo Gu, Yadan Du, Zhihui Zhou, Wenlong Li, Xiaobo Zheng, Wenjing Cai, Tian Chang.

Spectral purification improves monitoring accuracy of the comprehensive growth evaluation index for film-mulched winter wheat [J]. >Journal of Integrative Agriculture, 2024, 23(5): 1523-1540.

[8] Xuan Li, Shaowen Wang, Yifan Chen, Danwen Zhang, Shanshan Yang, Jingwen Wang, Jiahua Zhang, Yun Bai, Sha Zhang.

Improved simulation of winter wheat yield in North China Plain by using PRYM-Wheat integrated dry matter distribution coefficient [J]. >Journal of Integrative Agriculture, 2024, 23(4): 1381-1392.

[9] YANG Wei-bing, ZHANG Sheng-quan, HOU Qi-ling, GAO Jian-gang, WANG Han-Xia, CHEN Xian-Chao, LIAO Xiang-zheng, ZHANG Feng-ting, ZHAO Chang-ping, QIN Zhi-lie.

Transcriptomic and metabolomic analysis provides insights into lignin biosynthesis and accumulation and differences in lodging resistance in hybrid wheat [J]. >Journal of Integrative Agriculture, 2024, 23(4): 1105-1117.

[10] Yingxia Dou, Hubing Zhao, Huimin Yang, Tao Wang, Guanfei Liu, Zhaohui Wang, Sukhdev Malhi.

The first factor affecting dryland winter wheat grain yield under various mulching measures: Spike number [J]. >Journal of Integrative Agriculture, 2024, 23(3): 836-848.

[11] Yonghui Fan, Boya Qin, Jinhao Yang, Liangliang Ma, Guoji Cui, Wei He, Yu Tang, Wenjing Zhang, Shangyu Ma, Chuanxi Ma, Zhenglai Huang.

Night warming increases wheat yield by improving pre-anthesis plant growth and post-anthesis grain starch biosynthesis [J]. >Journal of Integrative Agriculture, 2024, 23(2): 536-550.

[12] Wei Chen, Jingjuan Zhang, Xiping Deng.

Winter wheat yield improvement by genetic gain across different provinces in China [J]. >Journal of Integrative Agriculture, 2024, 23(2): 468-483.

[13] Wenqiang Wang, Xizhen Guan, Yong Gan, Guojun Liu, Chunhao Zou, Weikang Wang, Jifa Zhang, Huifei Zhang, Qunqun Hao, Fei Ni, Jiajie Wu, Lynn Epstein, Daolin Fu.

Creating large EMS populations for functional genomics and breeding in wheat [J]. >Journal of Integrative Agriculture, 2024, 23(2): 484-493.

[14] Changqin Yang, Xiaojing Wang, Jianan Li, Guowei Zhang, Hongmei Shu, Wei Hu, Huanyong Han, Ruixian Liu, Zichun Guo.

Straw return increases crop production by improving soil organic carbon sequestration and soil aggregation in a long-term wheat–cotton cropping system [J]. >Journal of Integrative Agriculture, 2024, 23(2): 669-679.

[15] Qiuyan Yan, Linjia Wu, Fei Dong, Shuangdui Yan, Feng Li, Yaqin Jia, Jiancheng Zhang, Ruifu Zhang, Xiao Huang.

Subsoil tillage enhances wheat productivity, soil organic carbon and available nutrient status in dryland fields [J]. >Journal of Integrative Agriculture, 2024, 23(1): 251-266.

No Suggested Reading articles found!